ContextLeprosy is a chronic granulomatous infectious disease process in humans primarily involving the skin, peripheral nerves, and nasal mucosa but capable of affecting any tissue or organ. The leprae bacilli were first observed by Hansen in 1868. Although this was the first bacterial human pathogen to be described, it continues to remain one of the least understood.AimsThe aim of the study was to evaluate oral and facial manifestations in patients affected with leprosy.Materials and methodsThe present study was performed with an aim of reviewing oral and facial manifestations in patients suffering from leprosy. For this, 150 patients suffering from lepromatous and tuberculoid forms of leprosy were included in the study. The study was approved by the ethical committee appointed by SIBAR Institute of Dental Sciences, Guntur. Permission was also taken from asylum management and the district leprosy officer to conduct the study. All study samples were patients diagnosed with Hansen's disease by a leprologist using a bacteriological index.ResultsIn the present study, oral and facial manifestations were observed more frequently in the lepromatous type of leprosy than in the tuberculoid form. Also, these manifestations were less pronounced in group I than in group II and were more in groups III and IV based on increased exposure to the disease process. Statistical analysis was performed using the c2 -test and P values were also found to be significant.ConclusionPresent day diagnostic protocols for early detection and treatment are effective in controlling the disease and in preventing further progression with severe orofacial manifestations. A dentist should be able to recognize these manifestations and treat them under the supervision of a leprologist. Protective care must be taken in treating the disease, although it should not be held as a nightmare as was considered previously.

Leprosy has been known since ancient times [1] and is considered an antique disease process [2]. It has been described as kushta roga in the Indian scenario. It has been present in the society since ages and infected people have been isolated from society because of their unsightly appearance and unacceptable deformities. It has been considered one of the major social stigmas, on which many reformers have done tremendous work. According to Sr Dr. Giovanna Lussa, 'Leprosy is aptly said to be a challenge'. Mahatmas Gandhi said, 'Leprosy work is not merely medical relief; it is transforming frustration of life into joy of dedication, personal ambition into selfless service', revealing the intensity of agony that these patients carry in their personal life. As commented by Mother Teresa, leprosy is actually not a medical disease but a disease with impact on the psyche of the patient. 'The biggest disease today is not leprosy or tuberculosis, but rather the feeling of being unwanted', said Mother Teresa.

Leprosy or Hansen's disease affects both men and women equally, irrespective of their caste, creed, or community. The causative agent of leprosy is Mycobacterium leprae (M. leprae), which was discovered first in the year 1873 by Armauer Gerhard Hansen [3]. It is unfortunate that, despite being discovered early, the causative agent of this chronic infectious and debilitating disease has not been cultured to date, in vivo as well as ex vivo.

M. leprae is a Gram-negative bacillus, acid fast in nature [4],[5],[6],[7]. It principally affects the low temperature zones in the body, primarily the skin, peripheral nerves, and nasal mucosa, while also involving muscles, eyes, bones, testes, internal organs and sometimes even oral cavity.

The disease is fortunately of low infectivity, but is seen as one of the most crippling disorders associated with social stigma because it causes deformities in the affected individuals leading to major esthetic consequences and social problems rather than fatality of the sufferers.

The clinical manifestations of leprosy are so varied and diverse that they can mimic a variety of unrelated diseases. The spectrum of clinical manifestations depends upon the immune status of the patient. Skin lesions include a single or few flattened hypopigmented areas to raised erythematous patches or plaques. After a period of hyperesthesia, the lesions are seen to reveal hypoesthesia or anesthesia. Presentation may vary from an insignificant skin or oral lesion to an extensive disease process leading to profound disability and deformities [5].

Various types of specific and nonspecific intraoral lesions have been reported, including infiltration of tissues to ulcerations, perforations, and yellowish to red nodules [8]. Orofacial manifestations are very important in understanding the disease stage, its varied manifestations and complications. Oral and nasal lesions in leprosy are probably the most significant source of the spread of bacilli and the transmission of the disease as viable bacilli have been detected in the lesions seen in these areas. The anterior face is particularly affected in these patients, with severe destruction in some patients often involving the maxilla.

The diagnosis of leprosy is made from the characteristic clinical picture itself, which is not pathognomonic but suggestive. However, it has to be and should be complemented with skin bacilloscopy and histopathology. Involvement of the oral cavity in leprosy ranges from 19 to 60% and is seen more commonly in the lepromatous variant of leprosy. Often the orofacial manifestations seen in leprosy patients help in diagnosis at the initial stage itself. The dental surgeon is a competent person for identifying initial facial and oral changes and has an important role in the diagnosis of the disease process.

Leprosy has been broadly categorized into five types as per the Indian scenario: tuberculoid, borderline tuberculoid, borderline, borderline lepromatous, and lepromatous variants [9]. Among these, orofacial manifestations are more commonly seen in lepromatous leprosy [10],[11],[12],[13]. Another significant feature of lepromatous leprosy is the presence of numerous lesions that are laden with bacilli, making this variant of leprosy the most infective among the five types. With the advent of multidrug therapy (MDT), orofacial manifestations are being sparsely reported even in the lepromatous variant of leprosy.

Also, saliva is considered an important biological fluid of the body, although possible transmission of infection through saliva has not been studied much and has remained debatable in the past. Dental surgeons have always been in a dilemma while treating leprosy patients because of its contagious nature. Therefore, there has been a need for a clear study to establish the infective potential of saliva in patients with positive oral and facial manifestations. This would help dental surgeons take proper precautionary measures to perform various dental treatment procedures in affected patients.

Indeed in the present day prevalence of the disease, there is a strong need to re-evaluate the sites of occurrence, clinically and radiographically, in the disease process. Hence, the present clinical study was aimed to record and re-evaluate the oral and facial manifestations in leprosy patients with a corresponding microbiological examination of the salivary samples of infected patients in addition to a radiological assessment in the anterior maxilla to know the destructive patterns of this severely debilitating disease process.

Aims and objectives

To evaluate oral and facial manifestations in patients affected with leprosy;

To carry out microbiological examination of the saliva of patients affected with leprosy, having positive oral and facial manifestations for the presence of leprae bacilli; and

To carry out radiological evaluation of the maxillary anterior region in affected patients.

Patients and methods

The present study was performed to review the oral and facial manifestations in patients suffering from leprosy.

Source of data

A total of 150 patients suffering from lepromatous and tuberculoid forms of leprosy were included in the study. The study patients were those attending the leprosy wards of the Dermatology Department of Guntur General Hospital, Great Naltes, Morumpudi, and asylums with inpatients such as Bethany colony and Chengiskhan pet - Chilakaluri pet, in Guntur District.

The study was approved by the ethical committee appointed by SIBAR Institute of Dental Sciences, Guntur. Verbal consent was obtained from all patients before their inclusion into the study. Permission was also taken from asylum management and the district leprosy officer to conduct the study. All study patients had been diagnosed with Hansen's disease by a leprologist using a bacteriological index.

Selection criteria

Inclusion criteria

Age and sex were not considered as criteria in the study. The study sample was categorized into four groups according to the duration of exposure to the disease process: 0-3, 3-10, 10-20, and more than 20 years. All patients were diagnosed leprosy patients with lepromatous and tuberculoid variants and were under treatment for leprosy. Only those patients willing to undergo clinical, radiographic, and salivary sample evaluation were considered.

Exclusion criteria

Patients who were not willing to undergo clinical, radiographic, and saliva evaluation were excluded from the study. Pregnant leprosy patients and those with neurological deficits were also excluded from the study. Patients with any other diagnosable systemic condition showing orofacial changes were also excluded from the study.

All patients who fulfilled the inclusion criteria and were included in the study were assessed. They were made to sit comfortably on a chair. The examination was carried out under ample daylight. Details of the patients were entered into a specially designed proforma. All possible oral and facial manifestations were recorded and photographed. Patients in whom anterior maxilla was involved were considered for radiographic examination; periapical radiographs were taken using the bisecting angle technique to evaluate and assess bone loss around the maxillary central incisors and changes in the anterior nasal spine, followed by saliva collection. Only patients with positive oral and dental findings were considered for the salivary evaluation. Patients were asked to gargle with plain water to clean debris. A volume of 5 ml of whole salivary samples was then collected using the expectoration method in sterile bottles/cups. The collected salivary samples were stored at 4°C in storage boxes until the time of sample processing. The processed slides were visualized using a light microscope under oil immersion with ×100 resolution for microbiological evaluation. The clinical observations of various orofacial manifestations were presented in the form of tables and graphs, and were categorized on the basis of years of disease exposure and type of Hansen's disease.

Results

In the present study, out of 150 Hansen's patients, 89 (59.33%) were male and 61 (40.67%) were female. The total number of patients with positive oral and facial manifestations was 89 (100%), of whom 51 (57.30%) were male and 38 (42.70%) were female [Table 1]. All four groups were further analyzed on the basis of the type of Hansen's disease - namely, tuberculoid or lepromatous types. Hansen's patients were categorized into four groups (I, II, III, and IV) on the basis of their duration of exposure to disease in years, 0-3 years (I), 3-10 years (II), 10-20 years (III), and more than 20 years (IV), respectively. Both types of disease were found more in group IV - 28 (36.36%) tuberculoid type and 49 (63.54%) lepromatous type - followed by group III - nine (81.82%) TL and two (18.18%) lepromatous - and groups II and I [Table 2]. Among these, in group IV, 26 (40.6%) patients were female and 38 (59.4%) were male with oral and facial manifestations, followed by group III with 11 (52.45) female and 10 (47.6%) male patients and group II with two (100%) male and group I with one (100%) female [Table 3]. Facial manifestations recorded were hypopigmented patches over facial skin, nodular skin eruptions, lagophthalmos, scanty eyebrows, scanty eyelashes, saddle nose, scarring of the tissues, leonine facies, and sagged ears. (Plate 1 [Additional file 1]) These manifestations were less pronounced in group I followed by group II and were more in groups III and IV. Of all the facial manifestations, scanty eyebrows (63.6%), scanty eyelashes (58.4%), saddle nose (66.2%), and sagged ears (76.6%) were more predominant than hypopigmented patches over facial skin (7.8%), nodular eruptions over the skin (9.1%), lagophthalmos, scarring of the tissues, and leonine facies. The facial manifestations were observed with more frequency in lepromatous type of leprosy than in tuberculoid form and the predominant manifestations in these groups were scanty eyelashes (83.3%), scanty eyebrows (90.0%), saddle nose appearance (86.7%), and sagged ears (88.3%) [Table 4]. Oral manifestations recorded were pinkish discoloration of teeth, circumferential hypoplasia, shortened roots, depapillation of the dorsal aspect of the tongue, fissured tongue, and fibrosis of the soft palate and uvula (Plate 2 [Additional file 2]). These manifestations were also less pronounced in group I followed by II and were more in groups III and IV. Of all the oral manifestations, fissured tongue (54.5%) and circumferential hypoplasia (18.2%) were more predominant than other oral manifestations observed. The oral manifestations observed were more frequent in lepromatous type of leprosy than in tuberculoid form and the predominant manifestations in these groups were fissured tongue (68.3%) and circumferential hypoplasia (23.3%) (Graph 1a and b [Additional file 4]). In our study, out of 150 patients with leprosy, saliva samples were collected from 50 (33.33%) diseased patients who were having positive oral and facial manifestations. These samples were subjected to microbiological evaluation. Results were interpreted using a light microscope. Radiographic evaluation was also carried out for changes in anterior nasal spine and bone loss around the maxillary central incisors in 50 (33.33%) leprosy patients, followed by radiographic interpretation under bright illumination (Plate 3 [Additional file 3]). Statistical analysis was carried out using the c2 -test and P values were found to be significant.

Leprosy is a chronic, multi-system disease process caused by a gram negative and acid fast bacillus, Mycobacterium lepra. The clinico-pathological presentation of the disease is determined by the complex interaction between involved pathogen and the immune status of the patient [4]. It has a tendency to involve the oral and facial regions manifested with various signs and symptoms. After the advent of newer multidrug therapy regimens, this disease is considered to be eradicated from the society.

With this background, this study was undertaken to examine and re-evaluate the oral and facial manifestations in Hansen's patients. The study was conducted on 150 patients suffering with leprosy from various centres where patients were diagnosed by a leprologist into two polar variants, Tuberculoid leprosy and Lepromatous leprosy. Hence, patients with these two forms only were considered in the present study.

In the present study, age of the patients ranged from 18-80 years, with a mean age of 55 years. The number of male patients 89(60%) were higher than female patients 61(40%) in our study. This is almost consistent with the male and female ratio of 2:1 seen in India with regard to the studies of De Abreu et al.[14], Boggild et al.[15], and Deval N Vora et al.[16]. In contrast to these studies, Souza et al.[8] did not find any difference in the prevalence of leprosy in relation to the male and female patients in his study. No specific reason could be attributed for the predisposition of males towards getting afflicted with this infectious disease apart from the fact that males probably get more exposed to infection in the external environment.

Majority of Hansen's patients were seen in group IV, who were having more than 20 years of duration of disease compared to other three groups. Oral and facial manifestations were also found more commonly in the same group of patients i.e group IV suggesting that orofacial manifestations had increased with increase in duration of disease. These manifestations were found very rarely in patients with less duration of exposure suggesting early diagnosis and prompt treatment would control the disease progression to severe unaesthetic oral and facial changes seen late in the disease process. Also, in the present study, oral and facial manifestations were found with more prevalence in Lepromatous leprosy than the Tuberculoid leprosy in groups IV, III and II, however in group I, Tuberculoid form of leprosy was only noticed. Group IV showed diversity in the distribution of two polar forms of this disease, patients affected with lepromatous leprosy were 49(63.54%) and tuberculoid leprosy were 28(36.36%). This distribution of the sample among the types of leprosy was matching with the study conducted by Vania A Souza et al.[8]. This was in contrast however to the study conducted by Boggild et al.[15], where the rate of lepromatous leprosy was lower than other types of Hansen's disease.

Hansen's patients with less than 3 years of disease exposure manifested only hypoanaesthetic and hypopigmented patches over facial skin. Patients with more than 20 years of disease exposure manifested various facial features, which were in the decreasing order of prevalence, seen as sagged ears (76.6%), saddle nose deformity (66.2%), scanty eyelashes (63.6%), scanty eyebrows (58.4%) and nodular skin eruptions (9.1%). Saddle nose deformity was prevalent due to the early involvement of nasal mucosa because of it being low temperature area in the body and leprae bacilli having an affinity towards such areas. Also, it leads to an earlier destruction of nasal and alar cartilages leading to extensive destruction of the anterior face compromising facial aesthetics and spread of infection to the underlying maxillary region [17]. Reason attributed for sagged ears is said to be an infiltration of the ear lobules and helices with the bacilli which is responsible for the thinning and sagging of the ears, sometimes associated with degenerative changes in the cartilaginous tissues of the ear leading to deformities. Nodular eruptions were very few in occurrence in this study but older literature revealed their frequent occurrence. This might be because of the same reason cited earlier responsible for the lesser formations of such globi because of the recent invents of the newer drug regimens. Hence, the disease had not manifested with severe facial changes in the present study.

Negligible oral changes have been found in recently affected patients with upto 10 years of disease exposure. The predominant oral changes included fissured tongue (37.3%), circumferential hypoplasia (14.0%), loss of maxillary central incisors (11.56%) and depapillation of the tongue (6.7%). Reason attributed for predominance of fissured tongue was non-specific. This might not be directly related to the disease progression also. A peculiar observation of gingival recession with mild mobility of maxillary anterior teeth with healthy surrounding teeth and gingiva was found in many of the patients included. The maxillary anterior alveolar bone loss was found in radiographs and it increased as the disease advanced. The reason for this might be explained on the basis of infection of the nasal mucosa spreading locally, invading the anterior nasal spine and further down till the upper incisor region causing progressive bone loss, leading to loss of maxillary incisors in a high frequency of patients. These changes including saddle nose deformity, loss of anterior nasal spine with loss of maxillary anterior teeth gives an unaesthetic appearance of face in the affected Hansen's patients. As the older literature reveals, appearance of nodules, lepromas, in the oral cavity, were not observed in our study and perhaps, this could be explained on the basis of the fact that the disease had not progressed to such a severe stage and was controlled earlier.

Oral and facial changes recorded in the study were further analyzed with reference to the type of Hansen's disease. They were found to be commonly occurring in lepromatous form of leprosy than the tuberculoid form. Literature reveals that orofacial manifestations were more in lepromatous variant of leprosy than in other forms. This might be due to increased infective potential of lepromatous variant than other forms of leprosy. According to the study conducted by Taheri et al.[18] on 100 leprosy patients, facial manifestations found were atrophy of the anterior maxillary ridge (50%), facial deformity (85%) and atrophy of nasal spine (93%), the observations that were found in our study as well though in a much less prevalence. Also, the order of site specificity was not in favor with the WHO study [19] as well as the studies conducted by Motta et al.[20] and Brasil et al.[21] where dorsal aspect of the tongue, soft palate and uvula were the commoner areas of involvement [17]. In our study, atrophy of nasal spine was not found in tuberculoid form of leprosy. This was in accordance with the study conducted by Taheri et al.[18] Kumar et al. [22] in 1988 in his study found that oral manifestations of leprosy included papulo- nodular lesions and perforations involving the hard palate and soft palate. These findings were also not observed in our study and only fibrosis of the uvula was detected. Sujoy Ghosh et al. [4] described two rare case reports of pre-maxillary involvement and bilateral facial palsy along with skeletal and dental changes in the patients of leprosy. In our study, there was no pre-maxillary involvement with nodular eruptions but one case of facial palsy was detected. Also, the reason for its occurrence could not be attributed to Hansen's disease directly. Intraoral changes detected were circumferential hypoplasia, pinkish discoloration of teeth and few patients with facies leprosa [4]. Cobbled surface of the tongue was also detected commonly with an unusual involvement of the cheeks, floor of the mouth and buccal gingivae, findings which were in confirmation with the study conducted by Venkataraman BK [23]. Moller Christensen [24] demonstrated the frequent involvement of maxillary central incisors leading to loss of teeth, this finding was also found in our study although in patients suffering from lepromatous leprosy exclusively [23]. Radiological analysis of alveolar bone suggested Hansen's disease affecting only anterior bone of maxilla and leading to extensive interdental bone loss, sometimes followed by pre-mature exfoliation of the maxillary anterior teeth. The recorded findings in relation to saliva examination suggested that there were no leprae bacilli in the samples of saliva collected from Hansen's patients, confirming them to be non-infective.

The present study concluded therefore with the observations that orofacial manifestations were found with less frequency both qualitatively and quantitatively when compared with all old literature. Most of the manifestations that were found also could not be attributed directly to the disease process, stating them to be non-specific in nature as one of the probabilities. Also, the manifestations were found in a higher frequency in the patients with more years of duration of the disease process i.e. with more exposure to disease process. With the present day protocols of the treatment, the number of Hansen's patients with oral and facial manifestations was very rare in occurrence as the disease is not allowed to progress to the severe stages. It cannot be argued however that all these manifestations are reversible and curable; also, this being a fact that many patients on long duration of therapy had persisted oral and facial changes.

Summary and conclusion

Although Hansen's disease has been declared largely extinct from the country after the advent of MDT and newer, effective drug regimens, a few cases are still being reported in southern parts of India with less frequency. Its association with the oral cavity and facial region has been speculated over the past few decades. A number of studies have been conducted in southern India pertaining to this association. Thus, this study was planned to observe and re-evaluate the oral and facial manifestations of Hansen's disease and also to determine the infective potential of saliva in the patients with positive oral manifestations.

The sampled group comprised 150 patients diagnosed with tuberculoid or lepromatous types of leprosy by a leprologist. On the basis of the observations, the following conclusions were drawn:

The prevalence of leprosy has progressively reduced as individuals with less duration of exposure were very few in our study.

No intraoral manifestations were observed in the tuberculoid variant of leprosy in the study. Rather, fewer than expected manifestations were seen in the lepromatous variant of leprosy, implying the role of MDT in shifting the balance toward high host resistance and control of the disease process.

Incidence of active lesions in oral and facial regions was not detected in our study.

Established or long-standing cases showed some positive orofacial manifestations.

Sex predilection was more in men than in women (M: F=2 : 1 approximately).

All Hansen's patients did not develop orofacial manifestations in the initial stages. These manifestations increased with the duration of disease. Predominant facial changes observed were sagged ears, scanty eyelashes, eyebrows, and saddle nose deformity. Predominant oral changes included fissured tongue, circumferential hypoplasia, and loss of maxillary anterior teeth. As all patients who were under study were under treatment, no severe oral and facial manifestations or active lesions were encountered in our study.

Our study also proved that the salivary fluid of Hansen's disease patients posed no serious infective potential. Dental surgeons can institute general treatment protocols in Hansen's patients without any apprehension about transmission of the disease. Present day diagnostic protocols for early detection and treatment are effective in controlling the disease and preventing further progression with severe orofacial manifestations. A dentist should be able to recognize these manifestations and treat them under the supervision of a leprologist. However, protective care must be taken while treating the disease although it should not be held as a nightmare as considered previously.

Acknowledgements

The authors thank all patients who contributed to the study without whom this study would not have been feasible.